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(2009) 103, 364–367 & 2009 Macmillan Publishers Limited All rights reserved 0018-067X/09 $32.00 www.nature.com/hdy REVIEW The chromosomal of subobscura: a microevolutionary weapon to monitor global change

J Balanya`1, RB Huey2, GW Gilchrist3 and L Serra1 1Grup de Biologia Evolutiva, Departament de `tica, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalonia, Spain; 2Department of , University of Washington, Seattle, WA, USA and 3Department of Biology, College of William & Mary, Williamsburg, VA, USA

The Palaearctic species recently composition of . Indeed, the long-term variation of invaded the west coast of and North America. This this polymorphism shows a general increase in the frequency of invasion helped to corroborate the of the rich those inversions typical of low latitudes, with a corresponding chromosomal polymorphism of the species, as the same clinal decrease of those typical of populations closer to the poles. patterns than those observed in the original Palaearctic area Although the mechanisms underlying these changes are not were reproduced in the colonized areas in a relatively short well understood, the system remains a valid tool to monitor the period of time. The rapid response of this polymorphism to genetic impact of global warming on natural populations. environmental conditions makes it a good candidate to measure Heredity (2009) 103, 364–367; doi:10.1038/hdy.2009.86; the effect of the global rising of temperatures on the genetic published online 29 July 2009

Keywords: inversion polymorphism; global warming; thermal

Drosophila subobscura is a Palaearctic species that has been probably originated from individuals from the other studied extensively by and evolutionary (Ayala et al., 1989). for more than 70 years. In 1978 it was In the Palaearctic region, Prevosti (1974) and others discovered in Puerto Montt, Chile; within a few years it (reviewed in Krimbas and Loukas, 1980) determined that extended over much of Chile and into Argentina and the frequencies of many of the arrange- became the most common drosophilid in many places. In ments of D. subobscura vary in clinal patterns that 1982, it appeared in the American northwest, shortly are correlated with latitude. The association between thereafter it was found extensively distributed from climatic variables and the D. subobscura chromosomal southern British Columbia, through Washington and polymorphism has been interpreted as the result of Oregon, into central . The of adaptation, although some authors have argued that D. subobscura consists of five acrocentric , historical factors could explain the correlations without named A, J, U, E and O, plus a small dot–like invoking adaptive factors (Krimbas and Loukas, 1980). chromosome. Variations in sequence arrangement have The American populations, however, offer a rare been found in every one of the five large chromosomes: opportunity to test the role of selection in maintaining more than 80 different arrangements in total. There are the inversion-frequency clines: soon after the discovery differences between localities, but in every population of the species in America (3 years in the case of South most or all five chromosomes are polymorphic. The American populations), the frequencies of the chromo- frequencies of the various chromosomal arrangements some arrangements in nine South American and seven are remarkably similar in South America and in North North American populations were analysed (Prevosti America. The presence of the same 19 sequences, of 80 et al., 1988). Correlations between chromosomal arrange- known sequences, and in similar frequencies on both ment frequencies and latitude were calculated for these continents suggest that the two colonizations are not populations. Signs of these correlations are highly independent; the colonizers of one of the two continents coincident with those found in the Old World. The correlation coefficients are statistically significant for six chromosome arrangements in South America and for six Correspondence: Dr J Balanya`, Departament de Gene`tica, Facultat de in North America (Ayala et al., 1989). If we ignore the Biologia, Universitat de Barcelona, Av. Diagonal, 645. Annex planta 2, significance of individual correlations and consider only 08028 Barcelona, Spain. their sign, 12 out of 16 correlations have the same sign in E-mail: [email protected] all three continents. Not all these correlations are This paper is dedicated to A Prevosti on the occasion of his 90th anniversary. independent. If we exclude one per chromosome, 9 of Received 18 May 2009; accepted 26 May 2009; published online 12 correlations are of the same sign in all three 29 July 2009 continents. The probability of this coincidence being Chromosomal polymorphism in Drosophila subobscura J Balanya` et al 365 due to chance, as shown by a sign test, is Po0.001. Thus, arrangements of all chromosomes had changed signifi- the initial of chromosomal polymorphism on a cantly during this period in a systematic way: an increase continental scale was remarkably rapid and consistent. in the frequency of those arrangements typical of Although the signs of correlations between frequency southern latitudes and a decrease for those more and latitude were similar on all three continents, the common in northern latitudes were observed in all New World clines were nonetheless much shallower populations. These changes could be due to climatic than those in the Old World. Would the New World factors that are correlated with latitude, making the clines become steeper over time and, thus, continue to chromosomal composition of this species more ‘equator- converge on the Old World ones? To evaluate this ial’ (Sole´ et al., 2002). The same authors extended the possibility, additional samples were collected in North analysis to three Atlantic and three Central European and South America. This effort has resulted in a genetic populations, obtaining similar results (Balanya` et al., time series that now spans approximately two decades 2004). The genetic distances of the new populations to an on both continents and offers insights into the strength average southern population of reference had decreased and consistency of selection along latitudinal gradients in comparison with those of the old populations. Again, (Balanya` et al., 2003). Large samples were collected at six these changes could be the result of climatic factors that sites in South America in 1986 and 1999 and at seven are correlated with latitude; in particular, the assumption sites in North America in 1992 and 1994. Of the 18 gene that global warming was responsible for all the changes arrangements found on all three continents over the observed appeared rather likely. entire census period, between 14 and 17 (depending on Given the evidence of shifts in chromosome-arrange- the particular census), clines of the same sign on all ment frequency in Europe, might a similar change be three continents. It is interesting to note that the clines in taking place in the American colonizing populations, as South and North America had not become steeper over would be expected from global climate warming? Six time as expected, but remained distinctly shallower than South American and seven North American populations those in the Old World. In fact, none of the 18 gene were resampled in 1999 and 2004, respectively, and their arrangements on either continent showed a significant chromosomal polymorphism compared with those of the increase in slope. We speculate that the shallower slope corresponding first samples. A similar analysis that the may be due to the more limited number of inversions, one made in the Old World populations was then carried coupled with a general pattern of weak out. Table 1 shows the number of positive and negative (Mestres et al., 2001): all else being equal, more gene differences in each of the American subcontinents arrangements for a given chromosome allow more ways between the frequencies in the old and new samples to be a heterozygote. Coupled with graded selection for those arrangements showing significant positive or pressures along the plus some gene flow, the fewer negative correlation coefficients with latitude in Europe inversions would mean more shallow slopes. Indeed, the (Menozzi and Krimbas, 1992). These results show the slopes of the steepest clines (per each chromosome) in same trend as in the Old World: those arrangements the New World are suggestively correlated with the whose frequency shows a positive correlation coefficient number of gene arrangements (Pearson’s r ¼ 0.569, with latitude (potentially adapted to colder environ- t[8] ¼ 1.96, P ¼ 0.085) for that chromosome. ments) tend to be found at lower frequency in the new The adaptive value of the chromosomal polymorphism samples, whereas those with negative correlation coeffi- of D. subobscura and the capacity to respond very rapidly cient tend to increase their frequency. These long term and consistently to different environmental conditions changes detected in the chromosomal polymorphism of makes it a valuable tool to monitor global change. Newer D. subobscura in three discontinuous areas match those samples of inversion frequencies have been obtained for expected to take place in response to global warming. the colonizing populations since these first analyses: the Balanya` et al. (2006) decided to test more directly whether time series now spans approximately two decades for climate and chromosomes were, in fact, shifting in parallel. both North America and South America (Balanya` et al., They first used a principal component analysis to combine 2003). The various New World samples have clinal slopes arrangement frequencies into a single Chromosomal Index of the same sign as those in Europe, with minor (the first principal component), which explained 45.8% of fluctuations in the relative frequencies within a continent the total variability. The values of this index decreased with over time. This stable clinal pattern in the frequency of latitude on all three continents, such that high positive gene arrangements on all three continents allows us to values corresponded to a polymorphism associated with examine shifts in overall frequencies over time. warmer sites. The index increased between initial and final The first long-term studies on the inversion polymorphism samples in 24 of the 26 sites: thus, polymorphism of D. subobscura showed a trend toward a frequency decrease frequencies became more equatorial (warm adapted) at in standard gene arrangements and a frequency increase in most localities during the time interval considered. nonstandard gene arrangements (Frutos and Prevosti, 1984; Did climates in fact warm at these sites? To find out Gosteli, 1990; Orengo and Prevosti, 1996; Rodrı´guez-Trelles Balanya` et al. (2006) computed the first principal and Rodriguez, 1998; Rodrı´guez-Trelles et al., 1998). These component for weather data, using the mean monthly studies, however, were limited to one chromosome or to minimum and maximum temperatures at the nearest one population. Sole´ et al. (2002) extended these long- weather station for each sample locality. The first term studies to seven Mediterranean populations, principal component, explaining 79.8% of the variance, analyzing the frequencies of the chromosomal arrange- was the Temperature Index. It was negatively correlated ments of all the acrocentric chromosomes of the species. with latitude and increased over the sample period in 22 These authors compared the chromosomal polymorph- of the 26 localities (12 out of 13 in Europe, 5 out of 6 in ism of these populations with that of the same popula- South America and 5 out of 7 in North America), tions collected 26–35 years ago. The frequencies of gene indicating that temperature had, in fact, increased

Heredity Chromosomal polymorphism in Drosophila subobscura J Balanya` et al 366 Table 1 Long-term changes of the frequencies of chromosomal arrangements in the American populations New–old frequencies: Group 1: Arrangements with positive Group 2: Arrangements with negative correlation coefficient with latitude correlation coefficient with latitude

South North South and North South North South and North America America America America America America

Number of differences with positive sign 15 12 27 32 36 68 Number of differences with negative sign 22 31 53 16 20 36 Sign test NS Po0.05 Po0.05 Po0.10 Po0.10 Po0.02 Two groups are considered: one including all arrangements with positive correlation coefficients with latitude (more frequent towards the poles), and a second including all arrangements with negative correlation coefficients (more frequent towards the equator). For each chromosomal arrangement and for each population, the sign of the difference between the frequency of the arrangement in the new sample and in the old sample has been computed; thus, a positive sign indicates that the frequency of the arrangement has increased in that population during the period of time considered. The values given in the table correspond to the number of positive and negative signs scored in South American populations, North American populations and in both continents (pooled data). The significance of a sign test comparing the number of positive and negative differences within each group is also given. The P-values have been obtained using the sequential Bonferroni correction.

at most sites. Most interestingly, the changes in the is difficult to predict which inversions are expected to Chromosome Index paralleled those of the Temperature change their frequency. As a matter of fact, Anderson Index in 22 of 26 cases (Rayleigh test, Poo0.001), et al. (1991) were not able to detect major changes in consistent with the hypothesis that the changes observed data from 48 populations spanning more than 40 years. in the inversion polymorphism of D. subobscura were The only changes emerging from these data were an driven by the changes in temperature (Balanya` et al., increase in frequency of the arrangements Pikes 2006, Table 1 and Figure 2 therein). Peak and Tree Line in the Pacific Coast area. These Whether these systematic changes of the chromosomal arrangements are more abundant in eastern populations polymorphism are a consequence of local natural who are subject to higher mean temperatures selection or have been produced by migration from the (Schaeffer, 2008). lower latitudes (or both) remains an open question. The Although it seems likely that temperature has an fact that the species has been recently detected further important role in the distribution of the chromosomal north than previously in Europe supports the migration polymorphism in natural populations of D. subobscura, hypothesis (Saura, 1994). Similarly, the recent appearance attempts to reproduce the clinal patterns in the labora- of some low-latitude arrangements at high-latitude sites tory by culturing the flies at different temperature seems to point to the same direction (Sole´ et al., 2002; regimes have failed (reviewed in Krimbas, 1993; Santos Balanya` et al., 2004), although an effect of local adapta- et al., 2005). These results suggest that temperature alone tion cannot be excluded. might not be the selective agent. One alternative Similar rapid changes in the chromosomal polymor- proposed by Bradshaw and Holzapfel (2008) argues phism of other drosophila species in apparent response that ‘the increasing length of the growing season and to climate warming have been reported. The inversion the advance and delay of spring and winter, respectively, In(3R)Payne of D. melanogaster exhibits a North-South impose greater selection on populations cline in eastern Australia, with its frequency increasing than does the direct effect of temperature’. Nevertheless, towards the equator (Knibb et al., 1981). In samples these laboratory experiments cannot rule out a separated 20 years, a general increase of the frequency of direct effect of temperature, as they were conducted at the inversion in all populations, with a corresponding constant temperature in vials or small cages and do shift in elevation of the clinal pattern of about 71 towards not mimic the regime found in nature (Huey and the equator, is detected (Anderson et al., 2005; Umina Rosenzweig, 2009). et al., 2005). Levitan and Etges (2005) and Etges and In summary, the chromosomal polymorphism of Levitan (2008) also documented a decline in the D. subobscura is changing in step with climate in both frequencies of some northerly gene arrangements its original and colonized distribution areas. Although and an increase in several southern gene arrangements the mechanism underlying these changes are not yet well in North American populations of D. robusta in correla- understood, this system provides a powerful micro- tion with increasing temperatures. In D. pseudoobscura, evolutionary tool to monitor the genetic impact of the seasonal cycling of some arrangements of the third climate warming on natural populations. chromosome as well as the altitudinal clines detected in different localities of the North American Pacific Coast constitute evidence that this polymorphism Acknowledgements reacts to temperature, although the behaviour of the same chromosomal arrangement with respect to This work was financially supported by grant CGL2006- altitude or seasonal abundance may differ among 13423 from Ministerio de Ciencia y Tecnologia (LS), populations (Dobzhansky, 1948). In agreement with this grant 2005SGR-00995 from Generalitat de Catalunya, inconsistent behaviour of individual arrangements, NSF grants DEB0242313 (GWG), DEB9981598 (RBH), North-South clines are not evident in this species DEB9629822 (RBH & GWG), and NSF IOB-0416843 (Powell, 1992). Thus, in a scenario of global warming, it (RBH) and a Jeffress Research Grant (GWG).

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